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Yusuke Nishimura, Atsushi Natsume, and Howard J. Ginsberg

The authors describe a case of a 79-year-old man with a lumbar spinal dural arteriovenous fistula (DAVF) and isthmic spondylolisthesis at the same level. The patient's thoracic spine MRI study demonstrated swelling and increased T2 signal in the spinal cord and regional dilated perimedullary vessels. Lumbar spine MRI showed L-4 isthmic spondylolisthesis with severe bilateral L4–5 foraminal stenoses. Spinal angiography revealed a fistulous connection at the left L-4 nerve root sleeve between perimedullary veins and a dural branch of the L-4 radicular artery. Based on previous reports about secondary spinal DAVFs, the abnormal vascular communication likely developed secondary to the microtrauma and inflammation on the left L-4 nerve root sleeve, which was attributable to the isthmic spondylolisthesis. The authors performed disconnection of the arteriovenous shunt as well as an L4–5 decompression and posterior instrumented fusion with pedicle screws. The patient's postoperative course was uneventful, and he improved neurologically. It is important to bear in mind that a spinal DAVF may develop as a consequence of any sort of trauma or inflammation involving nerve roots. One should consider the concomitant treatment of both the spinal DAVF and the underlying pathology that may have given rise to the spinal DAVF.

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Kazuya Motomura, Masazumi Fujii, Satoshi Maesawa, Shunichiro Kuramitsu, Atsushi Natsume, and Toshihiko Wakabayashi

Alexia and agraphia are disorders common to the left inferior parietal lobule, including the angular and supramarginal gyri. However, it is still unclear how these cortical regions interact with other cortical sites and what the most important white matter tracts are in relation to reading and writing processes.

Here, the authors present the case of a patient who underwent an awake craniotomy for a left inferior parietal lobule glioma using direct cortical and subcortical electrostimulation. The use of subcortical stimulation allowed identification of the specific white matter tracts associated with reading and writing. These tracts were found as portions of the dorsal inferior frontooccipital fasciculus (IFOF) fibers in the deep parietal lobe that are responsible for connecting the frontal lobe to the superior parietal lobule. These findings are consistent with previous diffusion tensor imaging tractography and functional MRI studies, which suggest that the IFOF may play a role in the reading and writing processes. This is the first report of transient alexia and agraphia elicited through intraoperative direct subcortical electrostimulation, and the findings support the crucial role of the IFOF in reading and writing.

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Kuniaki Tanahashi, Kenji Uda, Yoshio Araki, Kazuhito Takeuchi, Jungsu Choo, Lushun Chalise, Kazuya Motomura, Fumiharu Ohka, Toshihiko Wakabayashi, and Atsushi Natsume

The presigmoid approach (PSA) is selected to obtain more lateral access to cerebellopontine angle tumors, brainstem cavernous malformations, or vertebrobasilar artery aneurysms than the standard retrosigmoid approach. However, mastoidectomy for the PSA can be considered time-consuming and to carry a higher risk of complications due to the anatomical complexity of the region. The authors established a method of minimized mastoidectomy focused on exposing Trautmann’s triangle as the corridor for the PSA while maximizing procedural simplicity and safety and maintaining a sufficient operative view. The authors present their method of minimized mastoidectomy in a cadaver dissection and operative cases, showing potential as a useful option for the PSA.

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Kenichiro Iwami, Hiroyuki Momota, Atsushi Natsume, Sayano Kinjo, Tetsuya Nagatani, and Toshihiko Wakabayashi

Object

Mouse models have been widely used in developing therapies for human brain tumors. However, surgical techniques such as bone drilling and skin suturing to create brain tumors in adult mice are still complicated. The aim of this study was to establish a simple and accurate method for intracranial injection of cells or other materials into mice.

Methods

The authors performed micro CT scans and skull dissection to assess the anatomical characteristics of the mouse postglenoid foramen. They then used xenograft and genetically engineered mouse models to evaluate a novel technique of percutaneous intracranial injection via the postglenoid foramen. They injected green fluorescent protein–labeled U87MG cells or virus-producing cells into adult mouse brains via the postglenoid foramen and identified the location of the created tumors by using bioluminescence imaging and histological analysis.

Results

The postglenoid foramen was found to be a well-conserved anatomical structure that allows percutaneous injection into the cerebrum, cerebellum, brainstem, and basal cistern in mice. The mean (± SD) time for the postglenoid foramen injection technique was 88 ± 15 seconds. The incidence of in-target tumor formation in the xenograft model ranged from 80% to 100%, depending on the target site. High-grade gliomas were successfully developed by postglenoid foramen injection in the adult genetically engineered mouse using virus-mediated platelet-derived growth factor B gene transfer. There were no procedure-related complications.

Conclusions

The postglenoid foramen can be used as a needle entry site into the brain of the adult mouse. Postglenoid foramen injection is a less invasive, safe, precise, and rapid method of implanting cells into the adult mouse brain. This method can be applied to both orthotopic xenograft and genetically engineered mouse models and may have further applications in mice for the development of therapies for human brain tumors.

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Toru Arima, Atsushi Natsume, Hisashi Hatano, Norimoto Nakahara, Mitsugu Fujita, Dai Ishii, Toshihiko Wakabayashi, Manabu Doyu, Tetsuro Nagasaka, and Jun Yoshida

✓ A rare case of chordoid meningioma in the lateral ventricle observed in an adult is reported. The first clinical manifestation of the disease was a prolonged fever of unknown origin. Abnormalities in the patient's blood chemistry, principally polyclonal hypergammaglobulinemia (immunoglobulin [Ig]G, IgA, and markedly IgE) and an elevated serum level of C-reactive protein, were associated with the disease. The tumor was histologically confirmed to be a chordoid meningioma, and its surgical removal resulted in complete resolution of the patient's symptoms. By combining reverse transcription—polymerase chain reaction and immunohistochemical analysis, it may be shown that cytokine production, including that of interleukin (IL)-6, IL-1β, and vascular endothelial growth factor, plays a role in the pathogenesis of chordoid meningioma associated with Castleman syndrome.

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Kazuya Motomura, Atsushi Natsume, Kentaro Iijima, Shunichiro Kuramitsu, Masazumi Fujii, Takashi Yamamoto, Satoshi Maesawa, Junko Sugiura, and Toshihiko Wakabayashi

OBJECTIVE

Maximum extent of resection (EOR) for lower-grade and high-grade gliomas can increase survival rates of patients. However, these infiltrative gliomas are often observed near or within eloquent regions of the brain. Awake surgery is of known benefit for the treatment of gliomas associated with eloquent regions in that brain function can be preserved. On the other hand, intraoperative MRI (iMRI) has been successfully used to maximize the resection of tumors, which can detect small amounts of residual tumors. Therefore, the authors assessed the value of combining awake craniotomy and iMRI for the resection of brain tumors in eloquent areas of the brain.

METHODS

The authors retrospectively reviewed the records of 33 consecutive patients with glial tumors in the eloquent brain areas who underwent awake surgery using iMRI. Volumetric analysis of MRI studies was performed. The pre-, intra-, and postoperative tumor volumes were measured in all cases using MRI studies obtained before, during, and after tumor resection.

RESULTS

Intraoperative MRI was performed to check for the presence of residual tumor during awake surgery in a total of 25 patients. Initial iMRI confirmed no further tumor resection in 9 patients (36%) because all observable tumors had already been removed. In contrast, intraoperative confirmation of residual tumor during awake surgery led to further tumor resection in 16 cases (64%) and eventually an EOR of more than 90% in 8 of 16 cases (50%). Furthermore, EOR benefiting from iMRI by more than 15% was found in 7 of 16 cases (43.8%). Interestingly, the increase in EOR as a result of iMRI for tumors associated mainly with the insular lobe was significantly greater, at 15.1%, than it was for the other tumors, which was 8.0% (p = 0.001).

CONCLUSIONS

This study revealed that combining awake surgery with iMRI was associated with a favorable surgical outcome for intrinsic brain tumors associated with eloquent areas. In particular, these benefits were noted for patients with tumors with complex anatomy, such as those associated with the insular lobe.

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Fumiaki Kanamori, Kinya Yokoyama, Akinobu Ota, Kazuhiro Yoshikawa, Sivasundaram Karnan, Mikio Maruwaka, Kenzo Shimizu, Shinji Ota, Kenji Uda, Yoshio Araki, Sho Okamoto, Satoshi Maesawa, Toshihiko Wakabayashi, and Atsushi Natsume

OBJECTIVE

Moyamoya disease (MMD) is a rare cerebrovascular disease characterized by progressive occlusion of the internal carotid artery and the secondary formation of collateral vessels. Patients with MMD have ischemic attacks or intracranial bleeding, but the disease pathophysiology remains unknown. In this study, the authors aimed to identify a gene expression profile specific to the intracranial artery in MMD.

METHODS

This was a single-center, prospectively sampled, retrospective cohort study. Microsamples of the middle cerebral artery (MCA) were collected from patients with MMD (n = 11) and from control patients (n = 9). Using microarray techniques, transcriptome-wide analysis was performed.

RESULTS

Comparison of MCA gene expression between patients with MMD and control patients detected 62 and 26 genes whose expression was significantly (p < 0.001 and fold change > 2) up- or downregulated, respectively, in the MCA of MMD. Gene set enrichment analysis of genes expressed in the MCA of patients with MMD revealed positive correlations with genes involved in antigen processing and presentation, the dendritic cell pathway, cytokine pathway, and interleukin-12 pathway, and negative correlations with genes involved in oxidative phosphorylation and DNA repair. Microarray analysis was validated by quantitative polymerase chain reaction.

CONCLUSIONS

Transcriptome-wide analysis showed upregulation of genes for immune responses and downregulation of genes for DNA repair and oxidative phosphorylation within the intracranial artery of patients with MMD. These findings may represent clues to the pathophysiology of MMD.

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Kazuya Motomura, Lushun Chalise, Hiroyuki Shimizu, Junya Yamaguchi, Tomohide Nishikawa, Fumiharu Ohka, Kosuke Aoki, Kuniaki Tanahashi, Masaki Hirano, Toshihiko Wakabayashi, and Atsushi Natsume

OBJECTIVE

This study aimed to evaluate the efficacy of levetiracetam (LEV) combined with perampanel (PER) therapy for intraoperative seizure treatment to determine whether a combination of LEV and PER can aid in the prevention of intraoperative intractable seizures during awake surgery.

METHODS

The authors performed a retrospective cohort study in 78 consecutive patients with glioma who underwent awake surgery using intraoperative direct electrical stimulation mapping. To prevent intraoperative seizures, 50 patients were treated with the antiepileptic drug LEV only (LEV group) from January 2017 to January 2019, while the remaining 28 patients were treated with LEV plus PER (LEV + PER group) between March 2019 and January 2020. LEV (1000–3000 mg) and/or PER (2–4 mg) were administered before the surgery.

RESULTS

Preoperative seizures with International League Against Epilepsy (ILAE) class II–VI occurred in 44% of the patients in the LEV group and in 35.7% of patients in the LEV + PER group, with no significant difference between groups (p = 0.319). Total intraoperative seizures occurred in 18 patients (36.0%) in the LEV therapy group and in 2 patients (7.1%) in the LEV + PER group (p = 0.009). Of these, there were no patients (0%) with intractable seizures in the LEV + PER group. Regarding factors that influence intraoperative seizures in glioma patients during awake brain surgery, multivariate logistic regression models revealed that the occurrence of intraoperative seizures was significantly related to the involvement of motor-related regions (positive vs negative, HR 6.98, 95% CI 1.71–28.56, p = 0.007), preoperative seizure (ILAE class II–VI vs ILAE class I, HR 4.44, 95% CI 1.22–16.11, p = 0.024), and LEV + PER group (positive vs negative, HR 0.07, 95% CI 0.01–0.44, p = 0.005). Treatment-related adverse effects were rare and mild, including sleepiness, tiredness, and dizziness in both treatment groups.

CONCLUSIONS

This study demonstrates that LEV + PER therapy is significantly associated with a lower risk of intraoperative seizures compared with LEV therapy alone in patients with glioma during awake brain mapping. These findings will help neurosurgeons conduct safe and reliable awake surgeries and reduce the rate of intraoperative intractable seizures during such procedures.

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Hiroyuki Shimizu, Kazuya Motomura, Fumiharu Ohka, Kosuke Aoki, Kuniaki Tanahashi, Masaki Hirano, Lushun Chalise, Tomohide Nishikawa, Junya Yamaguchi, Jun Yoshida, Atsushi Natsume, and Toshihiko Wakabayashi

OBJECTIVE

The current study aimed to evaluate the treatment outcomes and toxicities of patients with intracranial germ cell tumors (GCTs).

METHODS

This study retrospectively included 110 consecutive patients (70 patients in the germinomatous group and 40 patients in the nongerminomatous GCT [NGGCT] groups) receiving surgery, platinum-based chemotherapy, and radiotherapy for newly diagnosed primary intracranial GCTs. In the authors’ protocol, patients with GCTs were further divided into the following four groups: the germinomatous group and the NGGCT groups (mature teratoma, intermediate prognosis, or poor prognosis).

RESULTS

The median overall survival (OS) and progression-free survival (PFS) rates of the patients in the germinomatous group were significantly higher than those in the NGGCT group (p < 0.001). The 5-, 10-, and 20-year OS rates in the germinomatous group were 97.1%, 95.7%, and 93.2%, respectively, with a median follow-up of 11.0 years. On the contrary, the 5-, 10-, and 20-year OS rates in the NGGCT group were 67.3%, 63.4%, and 55.4%, respectively. The 5-, 10-, and 20-year PFS rates were 91.4%, 86.6%, and 86.6%, respectively, in the germinomatous group, whereas those of the NGGCT group were approximately 67.4%, 60.2%, and 53.5%, respectively. Based on the four types of classification in our study, the 5-, 10-, and 20-year OS rates in the NGGCT intermediate prognosis group were 78.9%, 71.8%, and 53.8%, respectively. On the contrary, the 3- and 5-year OS rates in the NGGCT poor prognosis group were 42.9% and 34.3%, respectively. Moreover, toxicities with the treatment of intracranial GCTs were found to be tolerable in the present study population. The multivariate survival models for OS in the NGGCT intermediate prognosis and poor prognosis groups demonstrated that only the alpha-fetoprotein status was significantly associated with worsened OS (HR 3.88, 95% CI 1.29–11.66; p = 0.02).

CONCLUSIONS

The authors found that platinum-based chemotherapy and radiotherapy result in favorable survival outcomes in patients with germinomatous GCTs. Clinical outcomes were still unfavorable in the NGGCT intermediate prognosis and poor prognosis groups; therefore, a new protocol that increases the survival rate of patients belonging in both groups should be considered.

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Hiroyuki Shimizu, Kazuya Motomura, Fumiharu Ohka, Kosuke Aoki, Kuniaki Tanahashi, Masaki Hirano, Lushun Chalise, Tomohide Nishikawa, Junya Yamaguchi, Jun Yoshida, Atsushi Natsume, and Toshihiko Wakabayashi

OBJECTIVE

The current study aimed to evaluate the treatment outcomes and toxicities of patients with intracranial germ cell tumors (GCTs).

METHODS

This study retrospectively included 110 consecutive patients (70 patients in the germinomatous group and 40 patients in the nongerminomatous GCT [NGGCT] groups) receiving surgery, platinum-based chemotherapy, and radiotherapy for newly diagnosed primary intracranial GCTs. In the authors’ protocol, patients with GCTs were further divided into the following four groups: the germinomatous group and the NGGCT groups (mature teratoma, intermediate prognosis, or poor prognosis).

RESULTS

The median overall survival (OS) and progression-free survival (PFS) rates of the patients in the germinomatous group were significantly higher than those in the NGGCT group (p < 0.001). The 5-, 10-, and 20-year OS rates in the germinomatous group were 97.1%, 95.7%, and 93.2%, respectively, with a median follow-up of 11.0 years. On the contrary, the 5-, 10-, and 20-year OS rates in the NGGCT group were 67.3%, 63.4%, and 55.4%, respectively. The 5-, 10-, and 20-year PFS rates were 91.4%, 86.6%, and 86.6%, respectively, in the germinomatous group, whereas those of the NGGCT group were approximately 67.4%, 60.2%, and 53.5%, respectively. Based on the four types of classification in our study, the 5-, 10-, and 20-year OS rates in the NGGCT intermediate prognosis group were 78.9%, 71.8%, and 53.8%, respectively. On the contrary, the 3- and 5-year OS rates in the NGGCT poor prognosis group were 42.9% and 34.3%, respectively. Moreover, toxicities with the treatment of intracranial GCTs were found to be tolerable in the present study population. The multivariate survival models for OS in the NGGCT intermediate prognosis and poor prognosis groups demonstrated that only the alpha-fetoprotein status was significantly associated with worsened OS (HR 3.88, 95% CI 1.29–11.66; p = 0.02).

CONCLUSIONS

The authors found that platinum-based chemotherapy and radiotherapy result in favorable survival outcomes in patients with germinomatous GCTs. Clinical outcomes were still unfavorable in the NGGCT intermediate prognosis and poor prognosis groups; therefore, a new protocol that increases the survival rate of patients belonging in both groups should be considered.